Non-reproductive effects of sex steroids: Their immunoregulatory role

Current Topics in Medicinal Chemistry

Volumn 11, Issue 13, 2011, Pages 1714-1727

  Muñoz Cruz, Samira ^a   Togno Pierce, Cristian ^b   Morales Montor, Jorge ^b  

^a INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Adaptive immunity; Infection; Innate immune response; Sex steroids; Sexual dimorphism

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; AUTOANTIBODY; CD40 ANTIGEN; CD69 ANTIGEN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FLUTAMIDE; GAMMA INTERFERON; HERMES ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 9; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROGESTERONE; SEX HORMONE; TAMOXIFEN; TESTOSTERONE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG;

ADAPTIVE IMMUNITY; ALLERGIC ENCEPHALOMYELITIS; ANESTRUS; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTHRITIS; ASTHMA; ASTROCYTE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BASOPHIL; BONE MARROW DERIVED DENDRITIC CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL MATURATION; CELL SELECTION; CELL SURVIVAL; CELLULAR IMMUNITY; COLLAGEN INDUCED ARTHRITIS; CYTOKINE PRODUCTION; DEGRANULATION; DENDRITIC CELL; DISEASE PREDISPOSITION; DOWN REGULATION; EOSINOPHIL; ESTRUS CYCLE; HUMAN; HUMORAL IMMUNITY; INFECTION; INNATE IMMUNITY; INTERFERON PRODUCING KILLER DENDRITIC CELL; LUPUS ERYTHEMATOSUS; LYMPH FOLLICLE; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MAST CELL; MENSTRUAL CYCLE; MULTIPLE SCLEROSIS; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; ORCHIECTOMY; OVARIECTOMY; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMA CELL; PLASMACYTOID DENDRITIC CELL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SEX DIFFERENCE; SPLEEN CELL; SYSTEMIC LUPUS ERYTHEMATOSUS; TH1 CELL; TH1 TH2 BALANCE; TH2 CELL; THYMOCYTE; UPREGULATION; UTERINE NATURAL KILLER CELL; VACCINATION; WOUND HEALING;

GONADAL STEROID HORMONES; HUMANS; IMMUNE SYSTEM; IMMUNE SYSTEM DISEASES; IMMUNOLOGIC FACTORS;

EID: 79959962195     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/156802611796117630     Document Type: Review

References (104)

1. Besedovsky, H. O.; del Rey, A. Immune-neuro-endocrine interactions: facts and hypotheses. Endocr. Rev., 1996, 17 (1), 64-102.
2. Armstrong, M. D.; Klein, J. R. Immune-endocrine interactions of the hypothalamus-pituitary-thyroid axis: integration, communication and homeostasis. Arch. Immunol. Ther. Exp., (Warsz) 2001, 49 (3), 231-237.
3. Chikanza, I. C.; Grossman, A. B. Reciprocal interactions between the neuroendocrine and immune systems during inflammation. Rheum. Dis. Clin. N. Am., 2000, 26 (4), 693-711.
4. Grossman, C. J.; Roselle, G. A.; Mendenhall, C. L. Sex steroid regulation of autoimmunity. J. Steroid Biochem. Mol. Biol., 1991, 40 (4-6), 649-59
5. Morales-Montor, J.; Baig, S.; Hallal-Calleros, C.; Damian, R. T. Taenia crassiceps: androgen reconstitution of the host leads to protection during cysticercosis. Exp. Parasitol., 2002, 100 (4), 209-216.
6. Jacobson, D. L.; Gange, S. J.; Rose, N. R.; Graham, N. M. Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin. Immunol. Immunopathol., 1997, 84 (3), 223-243
7. Cooper, G. S.; Stroehla, B. C. The epidemiology of autoimmune diseases. Autoimmun. Rev., 2003, 2 (3), 119-125.
8. Bouman, A.; Heineman, M. J.; Faas, M. M. Sex hormones and the immune response in humans. Hum. Reprod. Update, 2005, 11 (4), 411-423.
9. Zuk, M.; McKean, K. A. Sex differences in parasite infections: patterns and processes. Int. J. Parasitol., 1996, 26 (10), 1009-1023.
10. Bebo, B. F. Jr.; Fyfe-Johnson, A.; Adlard, K.; Beam, A. G.; Vandenbark, A. A.; Offner, H. Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. J. Immunol., 2001, 166 (3), 2080-2089
11. Da Silva, J. A. Sex hormones and glucocorticoids: interactions with the immune system. Ann. N. Y. Acad. Sci., 1999, 876, 102-117; discussion 117-8.
12. Venkatesh, J.; Peeva, E.; Xu, X.; Diamond, B. Cutting Edge: Hormonal milieu, not antigenic specificity, determines the mature phenotype of autoreactive B cells. J. Immunol., 2006, 176 (6), 3311-3314.
13. Ansar Ahmed, S.; Penhale, W. J.; Talal, N. Sex hormones, immune responses, and autoimmune diseases. Mechanisms of sex hormone action. Am. J. Pathol., 1985, 121 (3), 531-551.
14. Wira, C. R.; Sandoe, C. P. Sex steroid hormone regulation of IgA and IgG in rat uterine secretions. Nature, 1977, 268 (5620), 534-536.
15. Grimaldi, C. M.; Jeganathan, V.; Diamond, B. Hormonal regulation of B cell development: 17 beta-estradiol impairs negative selection of high-affinity DNA-reactive B cells at more than one developmental checkpoint. J. Immunol., 2006, 176 (5), 2703-2710.
16. Peeva, E.; Venkatesh, J.; Diamond, B. Tamoxifen blocks estrogeninduced B cell maturation but not survival. J. Immunol., 2005, 175 (3), 1415-1423.
17. Lu, F. X.; Abel, K.; Ma, Z.; Rourke, T.; Lu, D.; Torten, J.; McChesney, M.; Miller, C. J. The strength of B cell immunity in female rhesus macaques is controlled by CD8+ T cells under the influence of ovarian steroid hormones. Clin. Exp. Immunol., 2002, 128 (1), 10-20.
18. Kanda, N.; Tsuchida, T.; Tamaki, K. Testosterone suppresses anti-DNA antibody production in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Arthritis Rheum., 1997, 40 (9), 1703-1711.
19. Kanda, N.; Tsuchida, T.; Tamaki, K. Estrogen enhancement of anti-double-stranded DNA antibody and immunoglobulin G production in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Arthritis Rheum., 1999, 42 (2), 328-337.
20. Larosa, D. F.; Orange, J. S. 1. Lymphocytes. J. Allergy Clin. Immunol., 2008, 121 (2 Suppl), S364-369; quiz S412
21. Romagnani, S. Human Th17 cells. Arthritis Res. Ther., 2008, 10 (2), 206.
22. Salem, M. L.; Hossain, M. S.; Nomoto, K. Mediation of the immunomodulatory effect of beta-estradiol on inflammatory responses by inhibition of recruitment and activation of inflammatory cells and their gene expression of TNF-alpha and IFN-gamma. Int. Arch. Allergy Immunol., 2000, 121 (3), 235-245.
23. Gilmore, W.; Weiner, L. P.; Correale, J. Effect of estradiol on cytokine secretion by proteolipid protein-specific T cell clones isolated from multiple sclerosis patients and normal control subjects. J. Immunol., 1997, 158 (1), 446-451
24. Correale, J.; Arias, M.; Gilmore, W. Steroid hormone regulation of cytokine secretion by proteolipid protein-specific CD4+ T cell clones isolated from multiple sclerosis patients and normal control subjects. J. Immunol., 1998, 161 (7), 3365-3374.
25. Piccinni, M. P.; Giudizi, M. G.; Biagiotti, R.; Beloni, L.; Giannarini, L.; Sampognaro, S.; Parronchi, P.; Manetti, R.; Annunziato, F.; Livi, C. Progesterone favors the development of human T helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones. J. Immunol., 1995, 155 (1), 128-33.
26. Miyaura, H.; Iwata, M. Direct and indirect inhibition of Th1 development by progesterone and glucocorticoids. J. Immunol., 2002, 168 (3), 1087-1094.
27. Piccinni, M. P.; Maggi, E.; Romagnani, S. Role of hormonecontrolled T-cell cytokines in the maintenance of pregnancy. Biochem. Soc. Trans., 2000, 28 (2), 212-215.
28. Faas, M.; Bouman, A.; Moesa, H.; Heineman, M. J.; de Leij, L.; Schuiling, G. The immune response during the luteal phase of the ovarian cycle: a Th2-type response? Fertil Steril, 2000, 74 (5), 1008-1013.
29. Liva, S. M.; Voskuhl, R. R. Testosterone acts directly on CD4+ T lymphocytes to increase IL-10 production. J. Immunol., 2001, 167 (4), 2060-2067.
30. De Leon-Nava, M. A.; Nava, K.; Soldevila, G.; Lopez-Griego, L.; Chavez-Rios, J. R.; Vargas-Villavicencio, J. A.; Morales-Montor, J. Immune sexual dimorphism: effect of gonadal steroids on the expression of cytokines, sex steroid receptors, and lymphocyte proliferation. J. Steroid. Biochem. Mol. Biol., 2009, 113 (1-2), 57-64.
31. Beagley, K. W.; Gockel, C. M. Regulation of innate and adaptive immunity by the female sex hormones oestradiol and progesterone. FEMS Immunol. Med. Microbiol., 2003, 38 (1), 13-22.
32. Prieto, G. A.; Rosenstein, Y. Oestradiol potentiates the suppressive function of human CD4 CD25 regulatory T cells by promoting their proliferation. Immunology, 2006, 118 (1), 58-65.
33. Somerset, D. A.; Zheng, Y.; Kilby, M. D.; Sansom, D. M.; Drayson, M. T. Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory Tcell subset. Immunology, 2004, 112 (1), 38-43
34. Sasaki, Y.; Sakai, M.; Miyazaki, S.; Higuma, S.; Shiozaki, A.; Saito, S. Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod., 2004, 10 (5), 347-353.
35. Aluvihare, V. R.; Kallikourdis, M.; Betz, A. G. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol., 2004, 5 (3), 266-271.
36. Tai, P.; Wang, J.; Jin, H.; Song, X.; Yan, J.; Kang, Y.; Zhao, L.; An, X.; Du, X.; Chen, X.; Wang, S.; Xia, G.; Wang, B. Induction of regulatory T cells by physiological level estrogen. J. Cell Physiol., 2008, 214 (2), 456-464.
37. Latham, K. A.; Zamora, A.; Drought, H.; Subramanian, S.; Matejuk, A.; Offner, H.; Rosloniec, E. F. Estradiol treatment redirects the isotype of the autoantibody response and prevents the development of autoimmune arthritis. J. Immunol., 2003, 171 (11), 5820-5827.
38. Polanczyk, M. J.; Carson, B. D.; Subramanian, S.; Afentoulis, M.; Vandenbark, A. A.; Ziegler, S. F.; Offner, H. Cutting edge: estrogen drives expansion of the CD4+CD25+ regulatory T cell compartment. J. Immunol., 2004, 173 (4), 2227-2230.
39. Page, S. T.; Plymate, S. R.; Bremner, W. J.; Matsumoto, A. M.; Hess, D. L.; Lin, D. W.; Amory, J. K.; Nelson, P. S.; Wu, J. D. Effect of medical castration on CD4+ CD25+ T cells, CD8+ T cell IFN-gamma expression, and NK cells: a physiological role for testosterone and/or its metabolites. Am. J. Physiol. Endocrinol. Metab., 2006, 290 (5), E856-863.
40. Petri, M. A.; Mease, P. J.; Merrill, J. T.; Lahita, R. G.; Iannini, M. J.; Yocum, D. E.; Ginzler, E. M.; Katz, R. S.; Gluck, O. S.; Genovese, M. C.; Van Vollenhoven, R.; Kalunian, K. C.; Manzi, S.; Greenwald, M. W.; Buyon, J. P.; Olsen, N. J.; Schiff, M. H.; Kavanaugh, A. F.; Caldwell, J. R.; Ramsey-Goldman, R.; St Clair, E. W.; Goldman, A. L.; Egan, R. M.; Polisson, R. P.; Moder, K. G.; Rothfield, N. F.; Spencer, R. T.; Hobbs, K.; Fessler, B. J.; Calabrese, L. H.; Moreland, L. W.; Cohen, S. B.; Quarles, B. J.; Strand, V.; Gurwith, M.; Schwartz, K. E. Effects of prasterone on disease activity and symptoms in women with active systemic lupus erythematosus. Arthritis. Rheum., 2004, 50 (9), 2858-2868.
41. Mantovani, A.; Sica, A.; Sozzani, S.; Allavena, P.; Vecchi, A.; Locati, M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol., 2004, 25 (12), 677-686.
42. Ashcroft, G. S.; Mills, S. J. Androgen receptor-mediated inhibition of cutaneous wound healing. J. Clin. Invest., 2002, 110 (5), 615-24
43. Ahmadi, K.; McCruden, A. B. Macrophage may responses to androgen via its receptor. Med. Sci. Monit, 2006, 12 (1), BR15-20.
44. Khan, K. N.; Masuzaki, H.; Fujishita, A.; Kitajima, M.; Sekine, I.; Matsuyama, T.; Ishimaru, T. Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis. Hum. Reprod., 2005, 20 (7), 2004-2013.
45. Wang, Y.; Wang, L.; Zhao, J.; Qiao, Z. Estrogen, but not testosterone, down-regulates cytokine production in nicotineinduced murine macrophage. Methods Find Exp. Clin. Pharmacol., 2005, 27 (5), 311-316.
46. Subramanian, M.; Shaha, C. Up-regulation of Bcl-2 through ERK phosphorylation is associated with human macrophage survival in an estrogen microenvironment. J. Immunol., 2007, 179 (4), 2330-2338.
47. Routley, C. E.; Ashcroft, G. S. Effect of estrogen and progesterone on macrophage activation during wound healing. Wound Repair Regen, 2009, 17 (1), 42-50.
48. Gilliver, S. C.; Ruckshanthi, J. P.; Hardman, M. J.; Nakayama, T.; Ashcroft, G. S. Sex dimorphism in wound healing: the roles of sex steroids and macrophage migration inhibitory factor. Endocrinology, 2008, 149 (11), 5747-5757.
49. Chao, T. C.; Chao, H. H.; Chen, M. F.; Greager, J. A.; Walter, R. J. Female sex hormones modulate the function of LPS-treated macrophages. Am. J. Reprod. Immunol., 2000, 44 (5), 310-318
50. Huang, H.; He, J.; Yuan, Y.; Aoyagi, E.; Takenaka, H.; Itagaki, T.; Sannomiya, K.; Tamaki, K.; Harada, N.; Shono, M.; Shimizu, I.; Takayama, T. Opposing effects of estradiol and progesterone on the oxidative stress-induced production of chemokine and proinflammatory cytokines in murine peritoneal macrophages. J. Med. Invest., 2008, 55 (1-2), 133-141.
51. Juliet, P. A.; Hayashi, T.; Daigo, S.; Matsui-Hirai, H.; Miyazaki, A.; Fukatsu, A.; Funami, J.; Iguchi, A.; Ignarro, L. J. Combined effect of testosterone and apocynin on nitric oxide and superoxide production in PMA-differentiated THP-1 cells. Biochim. Biophys. Acta, 2004, 1693 (3), 185-191.
52. Gay-Andrieu, F.; Cozon, G. J.; Ferrandiz, J.; Peyron, F. Progesterone fails to modulate Toxoplasma gondii replication in the RAW 264.7 murine macrophage cell line. Parasite Immunol., 2002, 24 (4), 173-178.
53. D'Agostino, P.; Milano, S.; Barbera, C.; Di Bella, G.; La Rosa, M.; Ferlazzo, V.; Farruggio, R.; Miceli, D. M.; Miele, M.; Castagnetta, L.; Cillari, E. Sex hormones modulate inflammatory mediators produced by macrophages. Ann. N Y. Acad. Sci., 1999, 876, 426-429.
54. Rettew, J. A.; Huet-Hudson, Y. M.; Marriott, I. Testosterone reduces macrophage expression in the mouse of toll-like receptor 4, a trigger for inflammation and innate immunity. Biol. Reprod, 2008, 78 (3), 432-437.
55. Bekesi, G.; Kakucs, R.; Varbiro, S.; Racz, K.; Sprintz, D.; Feher, J.; Szekacs, B. In vitro effects of different steroid hormones on superoxide anion production of human neutrophil granulocytes. Steroids, 2000, 65 (12), 889-894.
56. Molloy, E. J.; O'Neill, A. J.; Grantham, J. J.; Sheridan-Pereira, M.; Fitzpatrick, J. M.; Webb, D. W.; Watson, R. W. Sex-specific alterations in neutrophil apoptosis: the role of estradiol and progesterone. Blood, 2003, 102 (7), 2653-2659.
57. Klinger, G.; Graser, T.; Mellinger, U.; Moore, C.; Vogelsang, H.; Groh, A.; Latterman, C. A comparative study of the effects of two oral contraceptives containing dienogest or desogestrel on the human immune system. Gynecol. Endocrinol., 2000, 14 (1), 15-24.
58. Garcia-Duran, M.; de Frutos, T.; Diaz-Recasens, J.; Garcia-Galvez, G.; Jimenez, A.; Monton, M.; Farre, J.; Sanchez de Miguel, L.; Gonzalez-Fernandez, F.; Arriero, M. D.; Rico, L.; Garcia, R.; Casado, S.; Lopez-Farre, A. Estrogen stimulates neuronal nitric oxide synthase protein expression in human neutrophils. Circ. Res., 1999, 85 (11), 1020-1026.
59. Pergola, C.; Dodt, G.; Rossi, A.; Neunhoeffer, E.; Lawrenz, B.; Northoff, H.; Samuelsson, B.; Radmark, O.; Sautebin, L.; Werz, O. ERK-mediated regulation of leukotriene biosynthesis by androgens: a molecular basis for gender differences in inflammation and asthma. Proc. Natl. Acad. Sci. USA, 2008, 105 (50), 19881-19886.
60. Bonini, S.; Lambiase, A.; Schiavone, M.; Centofanti, M.; Palma, L. A. Estrogen and progesterone receptors in vernal keratoconjunctivitis. Ophthalmology, 1995, 102 (9), 1374-1379
61. Lee, S. H. Uterine epithelial and eosinophil estrogen receptors in rats during the estrous cycle. Histochemistry, 1982, 74 (4), 443-452.
62. Hamano, N.; Terada, N.; Maesako, K.; Numata, T.; Konno, A. Effect of sex hormones on eosinophilic inflammation in nasal mucosa. Allergy Asthma Proc., 1998, 19 (5), 263-269.
63. Grunert, G.; Porcia, M.; Neumann, G.; Sepulveda, S.; Tchernitchin, A. N. Progesterone interaction with eosinophils and with responses already induced by oestrogen in the uterus. J. Endocrinol., 1984, 102 (3), 295-303.
64. Tchernitchin, A. N.; Barrera, J.; Arroyo, P.; Mena, M. A.; Vilches, K.; Grunert, G. Degranulatory action of estradiol on blood eosinophil leukocytes in vivo and in vitro. Agents Actions, 1985, 17 (1), 60-66.
65. Hellings, P. W.; Vandekerckhove, P.; Claeys, R.; Billen, J.; Kasran, A.; Ceuppens, J. L. Progesterone increases airway eosinophilia and hyper-responsiveness in a murine model of allergic asthma. Clin. Exp. Allergy, 2003, 33 (10), 1457-1463.
66. Mikhak, Z.; Luster, A. D. The emergence of basophils as antigenpresenting cells in Th2 inflammatory responses. J. Mol. Cell Biol., 2009, 1 (2), 69-71
67. Wynn, T. A. Basophils trump dendritic cells as APCs for T(H)2 responses. Nat. Immunol., 2009, 10 (7), 679-681.
68. Cocchiara, R.; Albeggiani, G.; Di Trapani, G.; Azzolina, A.; Lampiasi, N.; Rizzo, F.; Geraci, D. Modulation of rat peritoneal mast cell and human basophil histamine release by estrogens. Int. Arch. Allergy Appl. Immunol., 1990, 93 (2-3), 192-197.
69. Schroeder, J. T.; MacGlashan, D. W. Jr.; MacDonald, S. M.; Kagey-Sobotka, A.; Lichtenstein, L. M. Regulation of IgEdependent IL-4 generation by human basophils treated with glucocorticoids. J. Immunol., 1997, 158 (11), 5448-5454.
70. Sapino, A.; Cassoni, P.; Ferrero, E.; Bongiovanni, M.; Righi, L.; Fortunati, N.; Crafa, P.; Chiarle, R.; Bussolati, G. Estrogen receptor alpha is a novel marker expressed by follicular dendritic cells in lymph nodes and tumor-associated lymphoid infiltrates. Am. J. Pathol., 2003, 163 (4), 1313-1320
71. Paharkova-Vatchkova, V.; Maldonado, R.; Kovats, S. Estrogen preferentially promotes the differentiation of CD11c+ CD11b(intermediate) dendritic cells from bone marrow precursors. J. Immunol., 2004, 172 (3), 1426-1436.
72. Carreras, E.; Turner, S.; Paharkova-Vatchkova, V.; Mao, A.; Dascher, C.; Kovats, S. Estradiol acts directly on bone marrow myeloid progenitors to differentially regulate GM-CSF or Flt3 ligand-mediated dendritic cell differentiation. J. Immunol., 2008, 180 (2), 727-738
73. Siracusa, M. C.; Overstreet, M. G.; Housseau, F.; Scott, A. L.; Klein, S. L. 17beta-estradiol alters the activity of conventional and IFN-producing killer dendritic cells. J. Immunol., 2008, 180 (3), 1423-1431.
74. Uemura, Y.; Liu, T. Y.; Narita, Y.; Suzuki, M.; Matsushita, S. 17 Beta-estradiol (E2) plus tumor necrosis factor-alpha induces a distorted maturation of human monocyte-derived dendritic cells and promotes their capacity to initiate T-helper 2 responses. Hum. Immunol., 2008, 69 (3), 149-157.
75. Yang, L.; Hu, Y.; Hou, Y. Effects of 17beta-estradiol on the maturation, nuclear factor kappa B p65 and functions of murine spleen CD11c-positive dendritic cells. Mol. Immunol., 2006, 43 (4), 357-366.
76. Butts, C. L.; Shukair, S. A.; Duncan, K. M.; Bowers, E.; Horn, C.; Belyavskaya, E.; Tonelli, L.; Sternberg, E. M. Progesterone inhibits mature rat dendritic cells in a receptor-mediated fashion. Int. Immunol., 2007, 19 (3), 287-296.
77. Galli, S. J.; Tsai, M. Mast cells: versatile regulators of inflammation, tissue remodeling, host defense and homeostasis. J. Dermatol. Sci., 2008, 49 (1), 7-19.
78. de Oliveira, A. P.; Domingos, H. V.; Cavriani, G.; Damazo, A. S.; Dos Santos Franco, A. L.; Oliani, S. M.; Oliveira-Filho, R. M.; Vargaftig, B. B.; de Lima, W. T. Cellular recruitment and cytokine generation in a rat model of allergic lung inflammation are differentially modulated by progesterone and estradiol. Am. J. Physiol. Cell Physiol., 2007, 293 (3), C1120-1128.
79. Padilla, L.; Reinicke, K.; Montesino, H.; Villena, F.; Asencio, H.; Cruz, M.; Rudolph, M. I. Histamine content and mast cells distribution in mouse uterus: the effect of sexual hormones, gestation and labor. Cell Mol. Biol., 1990, 36 (1), 93-100
80. Vasiadi, M.; Kempuraj, D.; Boucher, W.; Kalogeromitros, D.; Theoharides, T. C. Progesterone inhibits mast cell secretion. Int. J. Immunopathol. Pharmacol., 2006, 19 (4), 787-794
81. Belot, M. P.; Abdennebi-Najar, L.; Gaudin, F.; Emilie, D.; Machelon, V. Progesterone increases csk homologous kinase in HMC-1560 human mast cells and reduces cell proliferation. J. Cell Biochem., 2007, 102 (5), 1271-1280.
82. Vliagoftis, H.; Dimitriadou, V.; Boucher, W.; Rozniecki, J. J.; Correia, I.; Raam, S.; Theoharides, T. C. Estradiol augments while tamoxifen inhibits rat mast cell secretion. Int. Arch. Allergy Immunol., 1992, 98 (4), 398-409.
83. Jeziorska, M.; Salamonsen, L. A.; Woolley, D. E. Mast cell and eosinophil distribution and activation in human endometrium throughout the menstrual cycle. Biol. Reprod., 1995, 53 (2), 312-320.
84. Pang, X.; Cotreau-Bibbo, M. M.; Sant, G. R.; Theoharides, T. C. Bladder mast cell expression of high affinity oestrogen receptors in patients with interstitial cystitis. Br. J. Urol., 1995, 75 (2), 154-161.
85. Zaitsu, M.; Narita, S.; Lambert, K. C.; Grady, J. J.; Estes, D. M.; Curran, E. M.; Brooks, E. G.; Watson, C. S.; Goldblum, R. M.; Midoro-Horiuti, T. Estradiol activates mast cells via a non-genomic estrogen receptor-alpha and calcium influx. Mol. Immunol., 2007, 44 (8), 1977-1985.
86. Nicovani, S.; Rudolph, M. I. Estrogen receptors in mast cells from arterial walls. Biocell, 2002, 26 (1), 15-24.
87. Shirasaki, H.; Watanabe, K.; Kanaizumi, E.; Konno, N.; Sato, J.; Narita, S.; Himi, T. Expression and localization of steroid receptors in human nasal mucosa. Acta. Otolaryngol., 2004, 124 (8), 958-963.
88. Zhao, X. J.; McKerr, G.; Dong, Z.; Higgins, C. A.; Carson, J.; Yang, Z. Q.; Hannigan, B. M. Expression of oestrogen and progesterone receptors by mast cells alone, but not lymphocytes, macrophages or other immune cells in human upper airways. Thorax, 2001, 56 (3), 205-211.
89. Kim, M. S.; Chae, H. J.; Shin, T. Y.; Kim, H. M.; Kim, H. R. Estrogen regulates cytokine release in human mast cells. Immunopharm. Immunotoxic., 2001, 23 (4), 495-504
90. Harnish, D. C.; Albert, L. M.; Leathurby, Y.; Eckert, A. M.; Ciarletta, A.; Kasaian, M.; Keith, J. C. Jr. Beneficial effects of estrogen treatment in the HLA-B27 transgenic rat model of inflammatory bowel disease. Am. J. Physiol. Gastrointest. Liver Physiol., 2004, 286 (1), G118-125.
91. Narita, S.; Goldblum, R. M.; Watson, C. S.; Brooks, E. G.; Estes, D. M.; Curran, E. M.; Midoro-Horiuti, T. Environmental estrogens induce mast cell degranulation and enhance IgE-mediated release of allergic mediators. Environ. Health Perspect., 2007, 115 (1), 48-52.
92. Orange, J. S.; Ballas, Z. K. Natural killer cells in human health and disease. Clin. Immunol., 2006, 118 (1), 1-10.
93. Henderson, T. A.; Saunders, P. T.; Moffett-King, A.; Groome, N. P.; Critchley, H. O. Steroid receptor expression in uterine natural killer cells. J. Clin. Endocrinol. Metab., 2003, 88 (1), 440-449.
94. Dosiou, C.; Giudice, L. C. Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr. Rev., 2005, 26 (1), 44-62.
95. Souza, S. S.; Castro, F. A.; Mendonca, H. C.; Palma, P. V.; Morais, F. R.; Ferriani, R. A.; Voltarelli, J. C. Influence of menstrual cycle on NK activity. J. Reprod. Immunol., 2001, 50 (2), 151-159.
96. Curran, E. M.; Berghaus, L. J.; Vernetti, N. J.; Saporita, A. J.; Lubahn, D. B.; Estes, D. M. Natural killer cells express estrogen receptor-alpha and estrogen receptor-beta and can respond to estrogen via a non-estrogen receptor-alpha-mediated pathway. Cell Immunol., 2001, 214 (1), 12-20.
97. Arruvito, L.; Giulianelli, S.; Flores, A. C.; Paladino, N.; Barboza, M.; Lanari, C.; Fainboim, L. NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis. J. Immunol., 2008, 180 (8), 5746-5753.
98. Bouman, A.; Moes, H.; Heineman, M. J.; de Leij, L. F.; Faas, M. M. Cytokine production by natural killer lymphocytes in follicular and luteal phase of the ovarian cycle in humans. Am. J. Reprod. Immunol., 2001, 45 (3), 130-134.
99. Gourdy, P.; Araujo, L. M.; Zhu, R.; Garmy-Susini, B.; Diem, S.; Laurell, H.; Leite-de-Moraes, M.; Dy, M.; Arnal, J. F.; Bayard, F.; Herbelin, A. Relevance of sexual dimorphism to regulatory T cells: estradiol promotes IFN-gamma production by invariant natural killer T cells. Blood, 2005, 105 (6), 2415-2420.
100. Lorenzo, J. A new hypothesis for how sex steroid hormones regulate bone mass. J. Clin. Invest., 2003, 111 (11), 1641-1643
101. Vertino, A. M.; Bula, C. M.; Chen, J. R.; Almeida, M.; Han, L.; Bellido, T.; Kousteni, S.; Norman, A. W.; Manolagas, S. C. Nongenotropic, anti-apoptotic signaling of 1alpha,25(OH)2-vitamin D3 and analogs through the ligand binding domain of the vitamin D receptor in osteoblasts and osteocytes. Mediation by Src, phosphatidylinositol 3-, and JNK kinases. J. Biol. Chem., 2005, 280 (14), 14130-14137.
102. Kousteni, S.; Chen, J. R.; Bellido, T.; Han, L.; Ali, A. A.; O'Brien, C. A.; Plotkin, L.; Fu, Q.; Mancino, A. T.; Wen, Y.; Vertino, A. M.; Powers, C. C.; Stewart, S. A.; Ebert, R.; Parfitt, A. M.; Weinstein, R. S.; Jilka, R. L.; Manolagas, S. C. Reversal of bone loss in mice by nongenotropic signaling of sex steroids. Science, 2002, 298 (5594), 843-846.
103. Leung, S. W.; Teoh, H.; Keung, W.; Man, R. Y. Non-genomic vascular actions of female sex hormones: physiological implications and signalling pathways. Clin. Exp. Pharmacol. Physiol., 2007, 34 (8), 822-826.
104. Fu, X. D.; Simoncini, T. Non-genomic sex steroid actions in the vascular system. Semin. Reprod. Med., 2007, 25 (3), 178-186.